International Journal of Pediatric Otorhinolaryngology 79 (2015) 532–536
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Predicting outcomes of balloon laryngoplasty in children with subglottic stenosis Melissa Avelino a, Rebecca Maunsell b,*, Isabela Jube´ Wastowski c a
Universidade Federal de Go´ias—UFG, Faculdade de Medicina, Rua 235 com a Primeira Radial s/n, Setor Universita´rio, CEP 74605-020 Goiaˆnia, GO, Brazil Hospital Estadual de Sumare´, Universidade Estadual de Campinas—UNICAMP, Av da Amizade, 2400, CEP 13175-490 Sumare´, SP, Brazil c Universidade Estadual de Goia´s - UEG, Rua 14, n. 625, CEP 75650000 - Morrinhos, GO, Brazil b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 4 August 2014 Received in revised form 14 January 2015 Accepted 19 January 2015 Available online 28 January 2015
The treatment of subglottic stenosis in children remains a challenge for the otolaryngologist and may involve procedures such as endoscopy, open surgery, and often both. In the recent past, high-pressure balloons have been used in endoscopic treatment due to their relative facility and high success rates. Objective: To report success rates in the treatment of acquired subglottic stenosis with balloon laryngoplasty in children and identify predictive factors for the success of the technique and its complications. Methods: Descriptive, prospective study of children who were diagnosed with acquired subglottic stenosis and underwent balloon laryngoplasty as the primary treatment. Results: Balloon laryngoplasty was performed in 48 children with an average age of 20.7 months: 31 presented with chronic subglottic stenosis and 17 with acute stenosis. Success rate was 100% for acute and 39% for chronic subglottic stenosis. Success was significantly associated with several factors, including recently acquired stenosis, initial grade of stenosis, younger patient age, and the absence of tracheotomy. Complications were transitory dysphagia observed in three children and a submucosal cyst in one of the patients. Conclusions: Balloon laryngoplasty may be considered as a first line of treatment for acquired subglottic stenosis. In acute cases, the success rate was 100%, and even though results are less promising in chronic cases, complications were not significant and the patients can undergo open surgery without contraindications. Predictive factors of success were acute stenosis, less severe grades of stenosis, younger patient age, and the absence of tracheotomy. ß 2015 Elsevier Ireland Ltd. All rights reserved.
Keywords: Subglottic stenosis Larynx Dilatation Children
1. Introduction In the past 30 years, mortality rates in neonatal intensive care units (NICU) have decreased due to advances in perinatal medicine [1]. As a consequence, prolonged intubation has become more frequent. Indications for tracheotomy in neonates are still complex and controversial; a decision to perform tracheotomy must be based on multiple factors and not only on the length of intubation period. Although the incidence of acquired subglottic stenosis (SGS) has decreased in children, SGS remains one of the most frequent causes of stridor and respiratory discomfort in this population [2]. Acquired
* Corresponding author. Tel.: +55 19981026581/+55 1932420088; fax: +55 1932420088. E-mail addresses: [email protected] (M. Avelino), [email protected] (R. Maunsell), [email protected] (I. Jube´ Wastowski). http://dx.doi.org/10.1016/j.ijporl.2015.01.022 0165-5876/ß 2015 Elsevier Ireland Ltd. All rights reserved.
SGS accounts for 90% of the cases diagnosed in children and is most frequently caused by prolonged tracheal intubation [3]. Treatment of acquired stenosis may involve endoscopic and/or open surgical procedures. Amongst the endoscopic techniques available, dilatation with high-pressure balloons or balloon laryngoplasty (BL) has been increasingly reported as a valuable therapeutic option worldwide. The use of other methods for dilatation of the stenotic area, such as those involving endotracheal tubes and broncoscopes, has not been well described in children and may add additional trauma to the already scarred and inflamed tissue. It must be considered that the instruments used for these procedures are not small enough to pass through the stenotic areas without significant force and trauma. Most reports on endoscopic treatment of SGS involve the use of laser therapy [4], which is classically indicated for low-grade, noncircumferential stenosis in children with less than 1 cm of vertical extension. Chueng and Chadha [5] in their systematic review of results for endoscopic treatment of SGS in children
M. Avelino et al. / International Journal of Pediatric Otorhinolaryngology 79 (2015) 532–536
reported that neither the high-pressure balloon or the rigid dilatation methods could be considered superior due to the lack of comparative studies between the two methods. Tracheotomy is an acceptable procedure and offers the best outcome when extubation fails due to acute SGS. This procedure is most successful when performed by a physician experienced in airway endoscopy diagnosis and treatment. Although tracheotomy immediately solves respiratory insufficiency and facilitates weaning from sedation drugs and mechanical ventilation, caring of small children with a tracheotomy at home can be an overwhelming and frightening experience. The possible complications of tracheotomy include suprastomal collapse, tracheal stenosis, persistent tracheal granulation tissue, and bleeding [2]. Additionally, the risk of cannula obstruction with a mucous plug and death both at home and in the hospital cannot be ignored. Chronic or mature SGS is successively treated with open neck reconstructive surgeries. In addition, laryngotracheoplasty and partial cricotracheal resections are effective alternative procedures. However, there is often a need for secondary procedures, which result in prolonged intensive care admission and prolonged intubation or tracheotomy, and both techniques have a potential for causing serious complications [6,7]. Experienced groups have reported high success rates for laryngotracheoplasty and partial cricotracheal ressection [7,8]. Nonetheless, this requires an organized and coordinated team to provide meticulous pre- and postoperative care that involves controlling comorbidities, weaning from sedation, management of unstable airways, recognition of complications, and quick resolution of these life-threatening conditions. However, the risks involved in these procedures, which include graft infections, dehiscence, sepsis and restenosis, cannot be ignored. Children with additional conditions such as pulmonary conditions, gastro-esophageal reflux, facial deformities, and neurological impairment have an increased potential for complications and failures, and these are not infrequent specially in children under two years of age [2]. For all these reasons, this type of surgery may be delayed in many children, leading to a long period of child and family deprivation from normal life. The management of such complex cases of SGS continues to present a significant challenge to the pediatric otolaryngologist. Balloon dilatation has been used to treat laryngeal and tracheal stenosis in children since the early 1980’s with encouraging results [9,10], particularly in immature, inflammatory scar tissue. Its main advantage compared to other methods of dilatation is that it promotes centrifuge expansion even in the presence of a very reduced lumen. The goal of balloon laryngoplasty is to mechanically interrupt the process of mature scar formation during the pathophysiology of acquired SGS [11]. Recently, Ang et al. [12] reported experimental data showing that balloon dilatation may significantly decrease tissue damage and therefore induce less scar tissue formation. Lang and Brietzke [13], in their systematic review and meta-analysis on BL as a treatment modality for SGS in children, concluded that high success rates can be seen in the short term and complications are rare. Additionally, the authors suggested that failures might be related to more severe grades of stenosis. The aim of this study was to investigate the success rate of BL as a primary treatment for acquired SGS in children, to report its complications and establish a set of factors that may be used to predict the success rate of the procedure. 2. Materials and methods 2.1. Subjects and staging of SGS We carried out a prospective evaluation of balloon dilatation protocols performed in children under 14 years of age, which were
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diagnosed with acquired SGS. We reviewed data of patients that underwent balloon laryngoplasty (BL) between August 2011 and April 2014 in two tertiary university hospitals: Hospital Estadual de Sumare´—Unicamp and Hospital da Crianc¸a de Goiaˆnia. Procedures were performed in each hospital by two surgeons with experience in pediatric airway endoscopy and approved by the Ethics Committee of each corresponding hospital. Written informed consent was obtained from all patients included in the study. Patients with follow-up periods less than three months and those who presented simultaneously with a laryngeal condition such as vocal cord mobility impairment or laryngomalacia or had undergone previous endoscopic and/or open reconstruction procedures were excluded from this study. The following data were extracted from the hospital protocols: patient age, endoscopic grading of SGS at the time of initial diagnosis, presence of tracheotomy, number of dilatation procedures, presence of comorbities, and complications and success rates of the procedures. Comorbidities that were considered included prematurity and severe pulmonary disease. The type of scar tissue was classified as follows: 1. acute subglottic stenosis—patients who were diagnosed and treated up to 30 days after extubation or tracheotomy as a result of failed extubation; 2. chronic subglottic stenosis—patients that were diagnosed and treated after more than 30 days of extubation or tracheotomy as a result of failed extubation. Myer and Cotton classification [14] (see Table 1) was used to establish the initial grade of stenosis, which was determined with respiratory endoscopy prior to dilatation using a 4-mm and 2.7-mm telescope and endotracheal tubes for calibration. 2.2. Balloon dilatation technique Unless the child was previously hospitalized, dilatation procedures were performed in the Day Case Surgery unit. Dilatations were always performed under general anesthesia alternating spontaneous breathing and apnea during balloon inflation when necessary. Three different brands of balloons with lengths varying from 20 mm to 30 mm were used, and the balloon diameter varied according to the age of the patient and the size of the airway. As a general rule, the approximate measure of the balloon diameter was determined by adding 2 mm to the external diameter of the appropriate endotracheal tube for a given patient. The time and number of inflations during the same procedure varied according to the size of the airway, pulmonary reserve, and/or perception of glottic and/or supraglottic edema secondary to the balloon. Inflation pressure varied from 2 to 15 atm with a tendency for the use of greater pressure levels during the last year Table 1 Data results for acute SGS, chronic SGS and the overall group of patients submitted to balloon dilatation. Acute No. patients Average age (months) Trach No trach Grade* I II III No. dilatations Success rate
17 4.2 24% 76% 6% 47% 47% 2 100%
Chronic
Overall
31 29.96 87% 13%
48 20.70 65% 35%
3% 10% 87% 2.4 39%
4% 23% 73% 2.3 60%
* Myer-Cotton classification (of Grade of stenosis), this could be removed since it has been explained in material and methods.
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of the study based on personal reports and communications with experienced colleagues in this field. Inflation was sustained for a period varying from one to 2 min or until oxygen saturation levels fell below 90%. Time between dilatation procedures varied from 15 to 60 days due to operating theatre availability, comorbidity decompensation, or other clinical temporary contraindications to general anesthesia. All procedures before and after balloon dilatation were recorded and airway calibration was carried out using endotracheal tubes at the beginning and at the end of each procedure when allowed by the diameter of the airway. Fig. 1 illustrates the endoscopic findings before (acute SGS), during, and after the dilatation procedure in a 4month-old patient without a tracheotomy. All children received anti-reflux medication, oral prednisolone, and corticosteroid nebulization treatment following the dilatation procedures. Patients who had a tracheotomy were discharged from the hospital after a period of 6 to 8 h if no further complications such as fever, dysphagia, or respiratory discomfort were observed. Caregivers were advised to return to the hospital if any of these symptoms presented in the following hours or days and a postoperative consultation was scheduled in a week. Patients without tracheotomy were kept in the hospital and additional adrenaline
nebulization was prescribed during the first 24 h following the procedures. Non-invasive ventilation through nasal–facial CPAP masks were used following extubation after discussion with the PICU team depending on the childs history of pulmonary and neurologic condition and length of entubation and sedation. Supplementary oxygen was also used through nasal–facial masks or hoods following extubation if necessary. Treatment was considered successful in patients with tracheotomies when decanulation was achieved or for patients without tracheotomies when respiratory symptoms were relieved and no further treatment was necessary. 2.3. Statistical methods All statistical analyses were carried out using the Graphpad Prism program (Version 5.0) and SYSTAT 13 (Version 13.00.05). The quantitative clinical variables and epidemiological data were compared with the Mann–Whitney U test. Comparative analyses between the qualitative variables were performed using the two-sided Fisher exact test. Logistic Regression was performed to determine if clinical variables were independent predictive factors to the success of the procedure. A p value of less than 0.05 was considered significant.
3. Results 3.1. Patients and staging of SGS A total of 48 children submitted to BL were included in the study. Seventeen were diagnosed with acute SGS, as previously defined, and 31 were diagnosed with chronic SGS. Mean patient age was 20.7 months (varying from one month to 11 years of age). At the time of treatment, 65% of the children had a tracheotomy. Grade I SGS was seen in 4%, grade II in 23%, and grade III in 73% of the 48 patients. Mean number of balloon dilatation procedures per patient was 2.3. 3.2. Complications associated with BL Complications occurred in four patients (8.3%). Three patients presented dysphagia as a complication of the dilation procedure and this was noted soon after the procedure. In two cases dysphagia was mild and transient and resolved within less than 24 h with conservative measures. In one case dysphagia was persistent and a feeding tube was used for three weeks. No secondary pulmonary complications occurred in any of the patients. One patient developed a submucosal retention cyst after dilation with a mild stridor, which resolved after resection of the cyst without further complications or need for airway interventions. 3.3. Success rate of BL and associated predictive factors for positive outcome
Fig. 1. acute Grade III SGS in a 4 month old child, (a) before balloon dilatation; (b) with balloon in place and inflated; (c) same patient, four months after balloon dilatation.
Overall success for the 48 patients evaluated rate was 60.41%. Success rate for the acute SGS group was 100% and for the chronic SGS group was 39%. Acute SGS was significantly related to successful outcome (p < 0.0001) (Fig. 2). The average time to follow-up was 7.8 months (varying from 3 to 15 months). In the case of chronic SGS the mean time interval between extubation or tracheotomy and dilation procedure was 19.8 months with a minimum of 1.3 months and maximum of 129 months. Mean time period between extubation or tracheotomy and dilatation was not related to success of the treatment (p = 0.85) but the presence of comorbidities in the chronic stenosis
M. Avelino et al. / International Journal of Pediatric Otorhinolaryngology 79 (2015) 532–536
Fig. 2. Correlation between chronic and acute SGS groups and success of BL (p < 0.0001).
group (prematurity and/or severe pulmonary disease) was significantly related to unsuccessful treatment (p = 0.0016). Younger age at time of treatment was significantly related with successful outcome (p = 0.0006). Nevertheless, for the group with chronic SGS, age was not related to the success rates (p = 0.66). The absence of a tracheotomy was also associated with better success rates (p < 0.0001) and this was also observed when the chronic SGS group alone was considered (p = 0.015). Logistic regression confirmed this to be an independent predictive factor of success with p = 0.007. Grade of stenosis was significantly related to success rates, lower grades had better chances of success with p = 0.0076 and the same tendency was observed in the chronic group (p = 0.08). Logistic regression confirmed grade of stenosis as independent predictive factor of success with p = 0.026. Number of balloon dilatation procedures was not significantly related to success of treatment (p = 0.38). A summary of the results can be appreciated on Table 1. 4. Discussion Treatment of SGS in the pediatric population is generally a very long and sometimes frustrating process for patients and their families. In our country frequently acute and chronic stenosis may have been treated with a tracheotomy without a precise diagnosis of the airway pathology or an alternative plan of treatment options. The presence of an otolaryngologist trained in the evaluation of pediatric airway in the pediatric intensive care unit (PICU) and NICU is essential to change this scenario. Tracheotomies may frequently be avoided as shown by the high success rates of BL for acute SGS in this and other studies [9–11]. Although tracheotomy resolves respiratory insufficiency it is a scary reality that completely changes the family dynamics having to deal with the life-threatening possibility of a mucus plug or displacement of the cannula. BL can be an excellent option in the treatment of acute SGS helping avoid tracheotomies even in very young infants, a finding that has been confirmed in previous studies of acute subglottic stenosis treated with BL also with 100% resolution of respiratory symptoms [9,10]. There is a possibility that good outcome can also be related to natural, favorable, history of some inflammatory stenosis and not only to the effects of BL. Nevertheless, BL is undoubtedly an excellent tool facilitating extubation and many times avoiding tracheotomy specially in small children that fail extubation due to the presence of acute inflammatory response of the subglottis to an endotracheal tube. Although there is a lack of reports on SGS in children treated with other forms of dilatation it is quite reasonable to predict that the shearing forces are significantly reduced by the use of high
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pressure balloons which also have the advantage of bypassing extremely tight stenosis. Worldwide use of high-pressure balloons have confirmed this to be an important tool in the treatment of SGS be it primarily or as an adjuvant method post airway reconstruction. Reported success rates for BL in the treatment of acquired SGS vary between 60% [15] and 100% [11,16–19]. Recently Blanchard et al. [18] have suggested that BL is a successful primary treatment for congenital SGS, in theory a poor indication for this since cartilage deformity is expected. Simpson et al. reported in 1982 [4] a series of patients treated for laryngeal and tracheal stenosis with CO2 laser. The authors found an association between poor outcome or failure of treatment involving CO2 laser and the following contributing factors: circumferential stenosis, scar contraction, vertical extension greater than 1 cm, tracheomalacia and loss of cartilage, previous history of severe bacterial infection associated with tracheotomy and posterior laryngeal inlet scarring with arytenoids fixation. In the present study some of these factors may have been present in the chronic SGS group and played a role to the failure of treatment in this group. The fact that younger age was associated with successful outcomes in our study was probably biased on the fact that the group of children with acute SGS were in fact significantly younger than the group with chronic SGS. Special care is needed when performing balloon dilatation in children who do not have a tracheotomy [20]. Spontaneous respiration with an obstructed glottis may lead to severe complications such as pulmonary edema. As with most of the pediatric airway interventions close interaction with the anesthesiologist team is crucial. Some children present extremely reactive airways and, particularly, in small infants BL may lead to coughing and dysphagia post operatively. Transient dysphagia observed in this group was, nevertheless, a minor complication and has not have been reported elsewhere. Open surgery remains the best treatment option for chronic SGS especially when associated with more advanced stenosis (grades III and IV) which tend to have more cartilaginous component to scar tissue. We were not surprised to find out that the grade of stenosis was associated with poorer results as has been previously reported. Nevertheless, even in the largest studies [8,21] where decannulation rates for laryngotracheal reconstruction (LTR) can be as high as 89% this may involve multiple procedures. Failure rates in a first procedure occurred in 33% of the same study [8,21]. In reports of grade IV SGS treatment, failure rates after first surgery can be as high as 70% with the mean time to achieving decannulation being 28 months [22]. This shows that, although this is the best treatment option, it is not a simple one. Previous reports [23] have shown quite poor results for chronic SGS treated with BL in smaller studies. Although the present study showed only a 39% success rate for chronic SGS, we believe that even in such cases BL should be attempted since no contraindications for further open surgery have been observed. Most reports of results with BL do not discriminate acute and chronic cases but some suggest [11] worse results for mature or chronic SGS. In the present report, there is no significant association between the time elapsed since the intubation event and the success of dilation treatment for chronic cases. Success rates are probably more related to grade of SGS and characteristics of the actual scar tissue. It is logical that fine, laminar scars would be more easily dilated than gross cartilaginous fibrosis. Nevertheless this is not a straightforward observation to make. We have found that response to balloon dilation may in fact help characterize the type of scar tissue present in a given case of SGS. Whigham et al. [15] reported an association of failure with balloon dilatation with other airway comorbidities; nevertheless, the authors studied a very heterogenous group of patients submitted to BL as primary treatment and as adjuvant treatment, making their findings
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somewhat inconclusive. Contrary to the present study Whigham et al. did not find any correlation between the age, grade of stenosis, scar characteristics (soft or fibrotic), and treatment success. Our results show that it is crucial to distinguish between acute and chronic cases when reporting results on treatment of scar tissue. Also, long-term follow-up is essential to confirm the efficacy of this treatment over time. Future studies are needed to answer the question as to whether the results are sustainable over time and maintained during child airway growth. In the present study, treatment failure for BL in chronic SGS was 61%, nevertheless most of the children markedly improved their ability to phonate and had intelligible speech after balloon dilatation despite not being able to be decannulated. This was also observed in a previous smaller study [23]. This was a very positive aspect of the treatment noted both by parents and children, making the wait for definite treatment through open surgery more bearable. When patients receive appropriate ventilation and in cases of good tissue reactivity, BL is quite a straightforward procedure. It allows the expansion of a tight stenosis since the dilator guide has a diameter of 2 mm, without the use of tearing shear forces and excessive manipulation of the airway as seen with other dilation methods. This technique also did not pose any contraindications to further reconstructive open surgeries to which some patients have been submitted. The number of times an airway is dilated should follow expertise and a critical analysis of the progression of the stenosis with documentation and objective airway calibration. Interestingly, this was confirmed by data reported in the present study, where success rates were not related to the number of dilations. Videodocumentation and calibration of the airway with tracheal tubes provides some objectiveness to the follow-up of these procedures allowing the surgeon to reevaluate the progress of the treatment before offering families false expectations or postponing open reconstructive surgery. Collectively our data offers strong support for a place for BL as primary treatment for acquired SGS in children. Future large studies with a comprehensive description of patients, stenosis, use of adjuvant topical treatment and long-term follow-up are needed and will provided the needed data to set certain standards of procedure. Description of acute or chronic scars is critical when analyzing results since this is an important predictive factor of treatment success rate. 5. Conclusions Balloon laryngoplasty may be considered as a first line treatment for both acute and chronic acquired SGS. Overall success rate of BL in this study was 60.4%. Success rate was 100% for acute cases and 39% for chronic cases of SGS. Complications were mild and occurred in 8.3% of the patients. Predictive factors of success in this study were: acute stenosis, absence of previous tracheotomy, lower grade of stenosis and for chronic cases
presence of comorbidities such as prematurity and/or severe pulmonary disease. References [1] T.H. Allen, I.M. Steven, Prolonged endotracheal intubation in infants and children, Br. J. Anaesth. 37 (8) (1965) 566–573. [2] P. Monnier, in: P Monnier (Ed.), Pediatric Airway Surgery: Management of Laryngotracheal Stenosis in Infants and Children, 2011th ed., Springer, Heidelberg, 2010, p. 371. [3] P.H. Holinger, S.L. Kutnick, J.A. Schild, L.D. Holinger, Subglottic stenosis in infants and children, Ann. Otol. Rhinol. Laryngol. 85 (Sep (5 Pt.1)) (1976) 591–599. [4] G.T. Simpson, M.S. Strong, G.B. Healy, S.M. Shapshay, C.W. Vaughan, Predictive factors of success or failure in the endoscopic management of laryngeal and tracheal stenosis, Ann. Otol. Rhinol. Laryngol. 91 (Jul (4 Pt 1)) (1982) 384–388. [5] K. Chueng, N.K. Chadha, Primary dilatation as a treatment for pediatric laryngotracheal stenosis: a systematic review, Int. J. Pediatr. Otorhinolaryngol. 77 (5) (2013) 623–628. [6] J.A. Matute, M.A. Villafruela, M.D. Delgado, F.J. Berchi, J. Vazquez, Surgery of subglottic stenosis in neonates and children, Eur. J. Pediatr. Surg. 10 (Oct (5)) (2000) 286–290. [7] D.R. White, R.T. Cotton, J.A. Bean, M.J. Rutter, Pediatric cricotracheal resection: surgical outcomes and risk factor analysis, Arch. Otolaryngol. Head Neck Surg. 131 (10) (2005) 896–899. [8] J.W. Ochi, J.N. Evans, C.M. Bailey, Pediatric airway reconstruction at Great Ormond Street: a ten-year review. I. Laryngotracheoplasty and laryngotracheal reconstruction, Ann. Otol. Rhinol. Laryngol. 101 (6) (1992) 465–468. [9] M. Avelino, E. Fernandes, Balloon laryngoplasty for subglottic stenosis caused by orotracheal intubation at a tertiary care pediatric hospital, Int. Arch. Otorhinolaryngol. 18 (2013) 39–42. [10] C. Schweiger, M.M. Smith, G. Kuhl, D. Manica, P.J.C. Marostica, Balloon laryngoplasty in children with acute subglottic stenosis: experience of a tertiary-care hospital, Braz. J. Otorhinolaryngol. 77 (Nov (6)) (2011) 711–715. [11] F. Durden, S.E. Sobol, Balloon laryngoplasty as a primary treatment for subglottic stenosis, Arch. Otolaryngol. Head Neck Surg. 133 (8) (2007) 772–775. [12] A.H. Ang, V.K. Modi, R. Raithatha, M.M. April, R.F. Ward, A pilot study of balloon dilation in an animal model resulting in cricoid cartilage fracture: implications for the stenotic pediatric airway, Laryngoscope 120 (10) (2010) 2094–2097. [13] M. Lang, S.E. Brietzke, A systematic review and meta-analysis of endoscopic balloon dilation of pediatric subglottic stenosis, Otolaryngol. Head Neck Surg. 150 (2013) 174–179 (Official Journal of American Academy of OtolaryngologyHead and Neck Surgery). [14] C.M. Myer, D.M. O’Connor, R.T. Cotton, Proposed grading system for subglottic stenosis based on endotracheal tube sizes, Ann. Otol. Rhinol. Laryngol. 103 (4 Pt 1) (1994) 319–323. [15] A.S. Whigham, R. Howell, S. Choi, M. Pen˜a, G. Zalzal, D. Preciado, Outcomes of balloon dilation in pediatric subglottic stenosis, Ann. Otol. Rhinol. Laryngol. 121 (7) (2012) 442–448. [16] J.L. Guarisco, C.J. Yang, Balloon dilation in the management of severe airway stenosis in children and adolescents, J. Pediatr. Surg. 48 (8) (2013) 1676–1681. [17] C. Hautefort, N. Teissier, P. Viala, T. Van Den Abbeele, Balloon dilation laryngoplasty for subglottic stenosis in children: eight years’ experience, Arch. Otolaryngol. Head Neck Surg. 138 (3) (2012) 235–240. [18] M. Blanchard, N. Leboulanger, B. Thierry, J.-P. Blancal, F. Glynn, F. Denoyelle, et al., Management specificities of congenital laryngeal stenosis: external and endoscopic approaches, Laryngoscope 124 (4) (2013) 1013–1018. [19] W.O. Collins, N. Kalantar, H.B. Rohrs, R.C. Silva, The effects of balloon dilation laryngoplasty in children with congenital heart disease, Arch Otolaryngol Head Neck Surg. 138 (12) (2012) 1136–1140. [20] A. Gungor, Balloon dilation of the pediatric airway: potential for disaster, Am. J. Otolaryngol. 33 (1) (2012) 147–149. [21] J.W. Ochi, J.N. Evans, C.M. Bailey, Pediatric airway reconstruction at Great Ormond Street: a ten-year review II. Revisional airway reconstruction, Ann. Otol. Rhinol. Laryngol. 101 (7) (1992) 595–597. [22] L.M. Gustafson, B.E. Hartley, R.T. Cotton, Acquired total (grade 4) subglottic stenosis in children, Ann. Otol. Rhinol. Laryngol. 110 (1) (2001) 16–19. [23] R. Maunsell, M.A.G. Avelino, Balloon laryngoplasty for acquired subglottic stenosis in children: predictive factors for success, Braz. J. Otorhinolaryngol. 80 (Sep (5)) (2014) 409–415.
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Predicting outcomes of balloon laryngoplasty in children with subglottic stenosis Melissa Avelino a, Rebecca Maunsell b,*, Isabela Jube´ Wastowski c a
Universidade Federal de Go´ias—UFG, Faculdade de Medicina, Rua 235 com a Primeira Radial s/n, Setor Universita´rio, CEP 74605-020 Goiaˆnia, GO, Brazil Hospital Estadual de Sumare´, Universidade Estadual de Campinas—UNICAMP, Av da Amizade, 2400, CEP 13175-490 Sumare´, SP, Brazil c Universidade Estadual de Goia´s - UEG, Rua 14, n. 625, CEP 75650000 - Morrinhos, GO, Brazil b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 4 August 2014 Received in revised form 14 January 2015 Accepted 19 January 2015 Available online 28 January 2015
The treatment of subglottic stenosis in children remains a challenge for the otolaryngologist and may involve procedures such as endoscopy, open surgery, and often both. In the recent past, high-pressure balloons have been used in endoscopic treatment due to their relative facility and high success rates. Objective: To report success rates in the treatment of acquired subglottic stenosis with balloon laryngoplasty in children and identify predictive factors for the success of the technique and its complications. Methods: Descriptive, prospective study of children who were diagnosed with acquired subglottic stenosis and underwent balloon laryngoplasty as the primary treatment. Results: Balloon laryngoplasty was performed in 48 children with an average age of 20.7 months: 31 presented with chronic subglottic stenosis and 17 with acute stenosis. Success rate was 100% for acute and 39% for chronic subglottic stenosis. Success was significantly associated with several factors, including recently acquired stenosis, initial grade of stenosis, younger patient age, and the absence of tracheotomy. Complications were transitory dysphagia observed in three children and a submucosal cyst in one of the patients. Conclusions: Balloon laryngoplasty may be considered as a first line of treatment for acquired subglottic stenosis. In acute cases, the success rate was 100%, and even though results are less promising in chronic cases, complications were not significant and the patients can undergo open surgery without contraindications. Predictive factors of success were acute stenosis, less severe grades of stenosis, younger patient age, and the absence of tracheotomy. ß 2015 Elsevier Ireland Ltd. All rights reserved.
Keywords: Subglottic stenosis Larynx Dilatation Children
1. Introduction In the past 30 years, mortality rates in neonatal intensive care units (NICU) have decreased due to advances in perinatal medicine [1]. As a consequence, prolonged intubation has become more frequent. Indications for tracheotomy in neonates are still complex and controversial; a decision to perform tracheotomy must be based on multiple factors and not only on the length of intubation period. Although the incidence of acquired subglottic stenosis (SGS) has decreased in children, SGS remains one of the most frequent causes of stridor and respiratory discomfort in this population [2]. Acquired
* Corresponding author. Tel.: +55 19981026581/+55 1932420088; fax: +55 1932420088. E-mail addresses: [email protected] (M. Avelino), [email protected] (R. Maunsell), [email protected] (I. Jube´ Wastowski). http://dx.doi.org/10.1016/j.ijporl.2015.01.022 0165-5876/ß 2015 Elsevier Ireland Ltd. All rights reserved.
SGS accounts for 90% of the cases diagnosed in children and is most frequently caused by prolonged tracheal intubation [3]. Treatment of acquired stenosis may involve endoscopic and/or open surgical procedures. Amongst the endoscopic techniques available, dilatation with high-pressure balloons or balloon laryngoplasty (BL) has been increasingly reported as a valuable therapeutic option worldwide. The use of other methods for dilatation of the stenotic area, such as those involving endotracheal tubes and broncoscopes, has not been well described in children and may add additional trauma to the already scarred and inflamed tissue. It must be considered that the instruments used for these procedures are not small enough to pass through the stenotic areas without significant force and trauma. Most reports on endoscopic treatment of SGS involve the use of laser therapy [4], which is classically indicated for low-grade, noncircumferential stenosis in children with less than 1 cm of vertical extension. Chueng and Chadha [5] in their systematic review of results for endoscopic treatment of SGS in children
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reported that neither the high-pressure balloon or the rigid dilatation methods could be considered superior due to the lack of comparative studies between the two methods. Tracheotomy is an acceptable procedure and offers the best outcome when extubation fails due to acute SGS. This procedure is most successful when performed by a physician experienced in airway endoscopy diagnosis and treatment. Although tracheotomy immediately solves respiratory insufficiency and facilitates weaning from sedation drugs and mechanical ventilation, caring of small children with a tracheotomy at home can be an overwhelming and frightening experience. The possible complications of tracheotomy include suprastomal collapse, tracheal stenosis, persistent tracheal granulation tissue, and bleeding [2]. Additionally, the risk of cannula obstruction with a mucous plug and death both at home and in the hospital cannot be ignored. Chronic or mature SGS is successively treated with open neck reconstructive surgeries. In addition, laryngotracheoplasty and partial cricotracheal resections are effective alternative procedures. However, there is often a need for secondary procedures, which result in prolonged intensive care admission and prolonged intubation or tracheotomy, and both techniques have a potential for causing serious complications [6,7]. Experienced groups have reported high success rates for laryngotracheoplasty and partial cricotracheal ressection [7,8]. Nonetheless, this requires an organized and coordinated team to provide meticulous pre- and postoperative care that involves controlling comorbidities, weaning from sedation, management of unstable airways, recognition of complications, and quick resolution of these life-threatening conditions. However, the risks involved in these procedures, which include graft infections, dehiscence, sepsis and restenosis, cannot be ignored. Children with additional conditions such as pulmonary conditions, gastro-esophageal reflux, facial deformities, and neurological impairment have an increased potential for complications and failures, and these are not infrequent specially in children under two years of age [2]. For all these reasons, this type of surgery may be delayed in many children, leading to a long period of child and family deprivation from normal life. The management of such complex cases of SGS continues to present a significant challenge to the pediatric otolaryngologist. Balloon dilatation has been used to treat laryngeal and tracheal stenosis in children since the early 1980’s with encouraging results [9,10], particularly in immature, inflammatory scar tissue. Its main advantage compared to other methods of dilatation is that it promotes centrifuge expansion even in the presence of a very reduced lumen. The goal of balloon laryngoplasty is to mechanically interrupt the process of mature scar formation during the pathophysiology of acquired SGS [11]. Recently, Ang et al. [12] reported experimental data showing that balloon dilatation may significantly decrease tissue damage and therefore induce less scar tissue formation. Lang and Brietzke [13], in their systematic review and meta-analysis on BL as a treatment modality for SGS in children, concluded that high success rates can be seen in the short term and complications are rare. Additionally, the authors suggested that failures might be related to more severe grades of stenosis. The aim of this study was to investigate the success rate of BL as a primary treatment for acquired SGS in children, to report its complications and establish a set of factors that may be used to predict the success rate of the procedure. 2. Materials and methods 2.1. Subjects and staging of SGS We carried out a prospective evaluation of balloon dilatation protocols performed in children under 14 years of age, which were
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diagnosed with acquired SGS. We reviewed data of patients that underwent balloon laryngoplasty (BL) between August 2011 and April 2014 in two tertiary university hospitals: Hospital Estadual de Sumare´—Unicamp and Hospital da Crianc¸a de Goiaˆnia. Procedures were performed in each hospital by two surgeons with experience in pediatric airway endoscopy and approved by the Ethics Committee of each corresponding hospital. Written informed consent was obtained from all patients included in the study. Patients with follow-up periods less than three months and those who presented simultaneously with a laryngeal condition such as vocal cord mobility impairment or laryngomalacia or had undergone previous endoscopic and/or open reconstruction procedures were excluded from this study. The following data were extracted from the hospital protocols: patient age, endoscopic grading of SGS at the time of initial diagnosis, presence of tracheotomy, number of dilatation procedures, presence of comorbities, and complications and success rates of the procedures. Comorbidities that were considered included prematurity and severe pulmonary disease. The type of scar tissue was classified as follows: 1. acute subglottic stenosis—patients who were diagnosed and treated up to 30 days after extubation or tracheotomy as a result of failed extubation; 2. chronic subglottic stenosis—patients that were diagnosed and treated after more than 30 days of extubation or tracheotomy as a result of failed extubation. Myer and Cotton classification [14] (see Table 1) was used to establish the initial grade of stenosis, which was determined with respiratory endoscopy prior to dilatation using a 4-mm and 2.7-mm telescope and endotracheal tubes for calibration. 2.2. Balloon dilatation technique Unless the child was previously hospitalized, dilatation procedures were performed in the Day Case Surgery unit. Dilatations were always performed under general anesthesia alternating spontaneous breathing and apnea during balloon inflation when necessary. Three different brands of balloons with lengths varying from 20 mm to 30 mm were used, and the balloon diameter varied according to the age of the patient and the size of the airway. As a general rule, the approximate measure of the balloon diameter was determined by adding 2 mm to the external diameter of the appropriate endotracheal tube for a given patient. The time and number of inflations during the same procedure varied according to the size of the airway, pulmonary reserve, and/or perception of glottic and/or supraglottic edema secondary to the balloon. Inflation pressure varied from 2 to 15 atm with a tendency for the use of greater pressure levels during the last year Table 1 Data results for acute SGS, chronic SGS and the overall group of patients submitted to balloon dilatation. Acute No. patients Average age (months) Trach No trach Grade* I II III No. dilatations Success rate
17 4.2 24% 76% 6% 47% 47% 2 100%
Chronic
Overall
31 29.96 87% 13%
48 20.70 65% 35%
3% 10% 87% 2.4 39%
4% 23% 73% 2.3 60%
* Myer-Cotton classification (of Grade of stenosis), this could be removed since it has been explained in material and methods.
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of the study based on personal reports and communications with experienced colleagues in this field. Inflation was sustained for a period varying from one to 2 min or until oxygen saturation levels fell below 90%. Time between dilatation procedures varied from 15 to 60 days due to operating theatre availability, comorbidity decompensation, or other clinical temporary contraindications to general anesthesia. All procedures before and after balloon dilatation were recorded and airway calibration was carried out using endotracheal tubes at the beginning and at the end of each procedure when allowed by the diameter of the airway. Fig. 1 illustrates the endoscopic findings before (acute SGS), during, and after the dilatation procedure in a 4month-old patient without a tracheotomy. All children received anti-reflux medication, oral prednisolone, and corticosteroid nebulization treatment following the dilatation procedures. Patients who had a tracheotomy were discharged from the hospital after a period of 6 to 8 h if no further complications such as fever, dysphagia, or respiratory discomfort were observed. Caregivers were advised to return to the hospital if any of these symptoms presented in the following hours or days and a postoperative consultation was scheduled in a week. Patients without tracheotomy were kept in the hospital and additional adrenaline
nebulization was prescribed during the first 24 h following the procedures. Non-invasive ventilation through nasal–facial CPAP masks were used following extubation after discussion with the PICU team depending on the childs history of pulmonary and neurologic condition and length of entubation and sedation. Supplementary oxygen was also used through nasal–facial masks or hoods following extubation if necessary. Treatment was considered successful in patients with tracheotomies when decanulation was achieved or for patients without tracheotomies when respiratory symptoms were relieved and no further treatment was necessary. 2.3. Statistical methods All statistical analyses were carried out using the Graphpad Prism program (Version 5.0) and SYSTAT 13 (Version 13.00.05). The quantitative clinical variables and epidemiological data were compared with the Mann–Whitney U test. Comparative analyses between the qualitative variables were performed using the two-sided Fisher exact test. Logistic Regression was performed to determine if clinical variables were independent predictive factors to the success of the procedure. A p value of less than 0.05 was considered significant.
3. Results 3.1. Patients and staging of SGS A total of 48 children submitted to BL were included in the study. Seventeen were diagnosed with acute SGS, as previously defined, and 31 were diagnosed with chronic SGS. Mean patient age was 20.7 months (varying from one month to 11 years of age). At the time of treatment, 65% of the children had a tracheotomy. Grade I SGS was seen in 4%, grade II in 23%, and grade III in 73% of the 48 patients. Mean number of balloon dilatation procedures per patient was 2.3. 3.2. Complications associated with BL Complications occurred in four patients (8.3%). Three patients presented dysphagia as a complication of the dilation procedure and this was noted soon after the procedure. In two cases dysphagia was mild and transient and resolved within less than 24 h with conservative measures. In one case dysphagia was persistent and a feeding tube was used for three weeks. No secondary pulmonary complications occurred in any of the patients. One patient developed a submucosal retention cyst after dilation with a mild stridor, which resolved after resection of the cyst without further complications or need for airway interventions. 3.3. Success rate of BL and associated predictive factors for positive outcome
Fig. 1. acute Grade III SGS in a 4 month old child, (a) before balloon dilatation; (b) with balloon in place and inflated; (c) same patient, four months after balloon dilatation.
Overall success for the 48 patients evaluated rate was 60.41%. Success rate for the acute SGS group was 100% and for the chronic SGS group was 39%. Acute SGS was significantly related to successful outcome (p < 0.0001) (Fig. 2). The average time to follow-up was 7.8 months (varying from 3 to 15 months). In the case of chronic SGS the mean time interval between extubation or tracheotomy and dilation procedure was 19.8 months with a minimum of 1.3 months and maximum of 129 months. Mean time period between extubation or tracheotomy and dilatation was not related to success of the treatment (p = 0.85) but the presence of comorbidities in the chronic stenosis
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Fig. 2. Correlation between chronic and acute SGS groups and success of BL (p < 0.0001).
group (prematurity and/or severe pulmonary disease) was significantly related to unsuccessful treatment (p = 0.0016). Younger age at time of treatment was significantly related with successful outcome (p = 0.0006). Nevertheless, for the group with chronic SGS, age was not related to the success rates (p = 0.66). The absence of a tracheotomy was also associated with better success rates (p < 0.0001) and this was also observed when the chronic SGS group alone was considered (p = 0.015). Logistic regression confirmed this to be an independent predictive factor of success with p = 0.007. Grade of stenosis was significantly related to success rates, lower grades had better chances of success with p = 0.0076 and the same tendency was observed in the chronic group (p = 0.08). Logistic regression confirmed grade of stenosis as independent predictive factor of success with p = 0.026. Number of balloon dilatation procedures was not significantly related to success of treatment (p = 0.38). A summary of the results can be appreciated on Table 1. 4. Discussion Treatment of SGS in the pediatric population is generally a very long and sometimes frustrating process for patients and their families. In our country frequently acute and chronic stenosis may have been treated with a tracheotomy without a precise diagnosis of the airway pathology or an alternative plan of treatment options. The presence of an otolaryngologist trained in the evaluation of pediatric airway in the pediatric intensive care unit (PICU) and NICU is essential to change this scenario. Tracheotomies may frequently be avoided as shown by the high success rates of BL for acute SGS in this and other studies [9–11]. Although tracheotomy resolves respiratory insufficiency it is a scary reality that completely changes the family dynamics having to deal with the life-threatening possibility of a mucus plug or displacement of the cannula. BL can be an excellent option in the treatment of acute SGS helping avoid tracheotomies even in very young infants, a finding that has been confirmed in previous studies of acute subglottic stenosis treated with BL also with 100% resolution of respiratory symptoms [9,10]. There is a possibility that good outcome can also be related to natural, favorable, history of some inflammatory stenosis and not only to the effects of BL. Nevertheless, BL is undoubtedly an excellent tool facilitating extubation and many times avoiding tracheotomy specially in small children that fail extubation due to the presence of acute inflammatory response of the subglottis to an endotracheal tube. Although there is a lack of reports on SGS in children treated with other forms of dilatation it is quite reasonable to predict that the shearing forces are significantly reduced by the use of high
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pressure balloons which also have the advantage of bypassing extremely tight stenosis. Worldwide use of high-pressure balloons have confirmed this to be an important tool in the treatment of SGS be it primarily or as an adjuvant method post airway reconstruction. Reported success rates for BL in the treatment of acquired SGS vary between 60% [15] and 100% [11,16–19]. Recently Blanchard et al. [18] have suggested that BL is a successful primary treatment for congenital SGS, in theory a poor indication for this since cartilage deformity is expected. Simpson et al. reported in 1982 [4] a series of patients treated for laryngeal and tracheal stenosis with CO2 laser. The authors found an association between poor outcome or failure of treatment involving CO2 laser and the following contributing factors: circumferential stenosis, scar contraction, vertical extension greater than 1 cm, tracheomalacia and loss of cartilage, previous history of severe bacterial infection associated with tracheotomy and posterior laryngeal inlet scarring with arytenoids fixation. In the present study some of these factors may have been present in the chronic SGS group and played a role to the failure of treatment in this group. The fact that younger age was associated with successful outcomes in our study was probably biased on the fact that the group of children with acute SGS were in fact significantly younger than the group with chronic SGS. Special care is needed when performing balloon dilatation in children who do not have a tracheotomy [20]. Spontaneous respiration with an obstructed glottis may lead to severe complications such as pulmonary edema. As with most of the pediatric airway interventions close interaction with the anesthesiologist team is crucial. Some children present extremely reactive airways and, particularly, in small infants BL may lead to coughing and dysphagia post operatively. Transient dysphagia observed in this group was, nevertheless, a minor complication and has not have been reported elsewhere. Open surgery remains the best treatment option for chronic SGS especially when associated with more advanced stenosis (grades III and IV) which tend to have more cartilaginous component to scar tissue. We were not surprised to find out that the grade of stenosis was associated with poorer results as has been previously reported. Nevertheless, even in the largest studies [8,21] where decannulation rates for laryngotracheal reconstruction (LTR) can be as high as 89% this may involve multiple procedures. Failure rates in a first procedure occurred in 33% of the same study [8,21]. In reports of grade IV SGS treatment, failure rates after first surgery can be as high as 70% with the mean time to achieving decannulation being 28 months [22]. This shows that, although this is the best treatment option, it is not a simple one. Previous reports [23] have shown quite poor results for chronic SGS treated with BL in smaller studies. Although the present study showed only a 39% success rate for chronic SGS, we believe that even in such cases BL should be attempted since no contraindications for further open surgery have been observed. Most reports of results with BL do not discriminate acute and chronic cases but some suggest [11] worse results for mature or chronic SGS. In the present report, there is no significant association between the time elapsed since the intubation event and the success of dilation treatment for chronic cases. Success rates are probably more related to grade of SGS and characteristics of the actual scar tissue. It is logical that fine, laminar scars would be more easily dilated than gross cartilaginous fibrosis. Nevertheless this is not a straightforward observation to make. We have found that response to balloon dilation may in fact help characterize the type of scar tissue present in a given case of SGS. Whigham et al. [15] reported an association of failure with balloon dilatation with other airway comorbidities; nevertheless, the authors studied a very heterogenous group of patients submitted to BL as primary treatment and as adjuvant treatment, making their findings
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somewhat inconclusive. Contrary to the present study Whigham et al. did not find any correlation between the age, grade of stenosis, scar characteristics (soft or fibrotic), and treatment success. Our results show that it is crucial to distinguish between acute and chronic cases when reporting results on treatment of scar tissue. Also, long-term follow-up is essential to confirm the efficacy of this treatment over time. Future studies are needed to answer the question as to whether the results are sustainable over time and maintained during child airway growth. In the present study, treatment failure for BL in chronic SGS was 61%, nevertheless most of the children markedly improved their ability to phonate and had intelligible speech after balloon dilatation despite not being able to be decannulated. This was also observed in a previous smaller study [23]. This was a very positive aspect of the treatment noted both by parents and children, making the wait for definite treatment through open surgery more bearable. When patients receive appropriate ventilation and in cases of good tissue reactivity, BL is quite a straightforward procedure. It allows the expansion of a tight stenosis since the dilator guide has a diameter of 2 mm, without the use of tearing shear forces and excessive manipulation of the airway as seen with other dilation methods. This technique also did not pose any contraindications to further reconstructive open surgeries to which some patients have been submitted. The number of times an airway is dilated should follow expertise and a critical analysis of the progression of the stenosis with documentation and objective airway calibration. Interestingly, this was confirmed by data reported in the present study, where success rates were not related to the number of dilations. Videodocumentation and calibration of the airway with tracheal tubes provides some objectiveness to the follow-up of these procedures allowing the surgeon to reevaluate the progress of the treatment before offering families false expectations or postponing open reconstructive surgery. Collectively our data offers strong support for a place for BL as primary treatment for acquired SGS in children. Future large studies with a comprehensive description of patients, stenosis, use of adjuvant topical treatment and long-term follow-up are needed and will provided the needed data to set certain standards of procedure. Description of acute or chronic scars is critical when analyzing results since this is an important predictive factor of treatment success rate. 5. Conclusions Balloon laryngoplasty may be considered as a first line treatment for both acute and chronic acquired SGS. Overall success rate of BL in this study was 60.4%. Success rate was 100% for acute cases and 39% for chronic cases of SGS. Complications were mild and occurred in 8.3% of the patients. Predictive factors of success in this study were: acute stenosis, absence of previous tracheotomy, lower grade of stenosis and for chronic cases
presence of comorbidities such as prematurity and/or severe pulmonary disease. References [1] T.H. Allen, I.M. Steven, Prolonged endotracheal intubation in infants and children, Br. J. Anaesth. 37 (8) (1965) 566–573. [2] P. Monnier, in: P Monnier (Ed.), Pediatric Airway Surgery: Management of Laryngotracheal Stenosis in Infants and Children, 2011th ed., Springer, Heidelberg, 2010, p. 371. [3] P.H. Holinger, S.L. Kutnick, J.A. Schild, L.D. Holinger, Subglottic stenosis in infants and children, Ann. Otol. Rhinol. Laryngol. 85 (Sep (5 Pt.1)) (1976) 591–599. [4] G.T. Simpson, M.S. Strong, G.B. Healy, S.M. Shapshay, C.W. Vaughan, Predictive factors of success or failure in the endoscopic management of laryngeal and tracheal stenosis, Ann. Otol. Rhinol. Laryngol. 91 (Jul (4 Pt 1)) (1982) 384–388. [5] K. Chueng, N.K. Chadha, Primary dilatation as a treatment for pediatric laryngotracheal stenosis: a systematic review, Int. J. Pediatr. Otorhinolaryngol. 77 (5) (2013) 623–628. [6] J.A. Matute, M.A. Villafruela, M.D. Delgado, F.J. Berchi, J. Vazquez, Surgery of subglottic stenosis in neonates and children, Eur. J. Pediatr. Surg. 10 (Oct (5)) (2000) 286–290. [7] D.R. White, R.T. Cotton, J.A. Bean, M.J. Rutter, Pediatric cricotracheal resection: surgical outcomes and risk factor analysis, Arch. Otolaryngol. Head Neck Surg. 131 (10) (2005) 896–899. [8] J.W. Ochi, J.N. Evans, C.M. Bailey, Pediatric airway reconstruction at Great Ormond Street: a ten-year review. I. Laryngotracheoplasty and laryngotracheal reconstruction, Ann. Otol. Rhinol. Laryngol. 101 (6) (1992) 465–468. [9] M. Avelino, E. Fernandes, Balloon laryngoplasty for subglottic stenosis caused by orotracheal intubation at a tertiary care pediatric hospital, Int. Arch. Otorhinolaryngol. 18 (2013) 39–42. [10] C. Schweiger, M.M. Smith, G. Kuhl, D. Manica, P.J.C. Marostica, Balloon laryngoplasty in children with acute subglottic stenosis: experience of a tertiary-care hospital, Braz. J. Otorhinolaryngol. 77 (Nov (6)) (2011) 711–715. [11] F. Durden, S.E. Sobol, Balloon laryngoplasty as a primary treatment for subglottic stenosis, Arch. Otolaryngol. Head Neck Surg. 133 (8) (2007) 772–775. [12] A.H. Ang, V.K. Modi, R. Raithatha, M.M. April, R.F. Ward, A pilot study of balloon dilation in an animal model resulting in cricoid cartilage fracture: implications for the stenotic pediatric airway, Laryngoscope 120 (10) (2010) 2094–2097. [13] M. Lang, S.E. Brietzke, A systematic review and meta-analysis of endoscopic balloon dilation of pediatric subglottic stenosis, Otolaryngol. Head Neck Surg. 150 (2013) 174–179 (Official Journal of American Academy of OtolaryngologyHead and Neck Surgery). [14] C.M. Myer, D.M. O’Connor, R.T. Cotton, Proposed grading system for subglottic stenosis based on endotracheal tube sizes, Ann. Otol. Rhinol. Laryngol. 103 (4 Pt 1) (1994) 319–323. [15] A.S. Whigham, R. Howell, S. Choi, M. Pen˜a, G. Zalzal, D. Preciado, Outcomes of balloon dilation in pediatric subglottic stenosis, Ann. Otol. Rhinol. Laryngol. 121 (7) (2012) 442–448. [16] J.L. Guarisco, C.J. Yang, Balloon dilation in the management of severe airway stenosis in children and adolescents, J. Pediatr. Surg. 48 (8) (2013) 1676–1681. [17] C. Hautefort, N. Teissier, P. Viala, T. Van Den Abbeele, Balloon dilation laryngoplasty for subglottic stenosis in children: eight years’ experience, Arch. Otolaryngol. Head Neck Surg. 138 (3) (2012) 235–240. [18] M. Blanchard, N. Leboulanger, B. Thierry, J.-P. Blancal, F. Glynn, F. Denoyelle, et al., Management specificities of congenital laryngeal stenosis: external and endoscopic approaches, Laryngoscope 124 (4) (2013) 1013–1018. [19] W.O. Collins, N. Kalantar, H.B. Rohrs, R.C. Silva, The effects of balloon dilation laryngoplasty in children with congenital heart disease, Arch Otolaryngol Head Neck Surg. 138 (12) (2012) 1136–1140. [20] A. Gungor, Balloon dilation of the pediatric airway: potential for disaster, Am. J. Otolaryngol. 33 (1) (2012) 147–149. [21] J.W. Ochi, J.N. Evans, C.M. Bailey, Pediatric airway reconstruction at Great Ormond Street: a ten-year review II. Revisional airway reconstruction, Ann. Otol. Rhinol. Laryngol. 101 (7) (1992) 595–597. [22] L.M. Gustafson, B.E. Hartley, R.T. Cotton, Acquired total (grade 4) subglottic stenosis in children, Ann. Otol. Rhinol. Laryngol. 110 (1) (2001) 16–19. [23] R. Maunsell, M.A.G. Avelino, Balloon laryngoplasty for acquired subglottic stenosis in children: predictive factors for success, Braz. J. Otorhinolaryngol. 80 (Sep (5)) (2014) 409–415.
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